Previous studies correlating ultrasound (US)-based optic nerve sheath diameter (ONSD) and intracranial pressure (ICP) in children were performed under general anesthesia. To apply ONSD in daily clinical routine, it is necessary to investigate patients awake. It is furthermore essential for ICP-assessment with ONSD to know if ONSD-ICP correlation varies within individuals. In this study, we report on the influence of wakefulness, method of ICP measurement, intraindividual correlations, and dynamic changes of ONSD and ICP after ICP decreasing therapy.
The overall study included 72 children with a median age of 5.2 years. US ONSD determination was performed immediately prior to invasive ICP measurement, and the mean binocular ONSD was compared to ICP. In 10 children, a minimum of 3 ONSD/ICP measurements were performed to investigate a correlation within subjects. In 30 children, measurements were performed before and after therapy.
Twenty-eight children were investigated awake with an excellent correlation of ONSD and ICP (r = 0.802, p < 0.01). In 10 children, at least three simultaneous ONSD and ICP measurements were performed. The intraindividual correlations were excellent (r = 0.795–1.0) however with strongly differing individual regression curves. The overall correlation within subjects was strong (r = 0.78, p < 0.01). After ICP decreasing therapy, all ONSD values decreased significantly (p < 0.01); however, there was no correlation between ∆ICP and ∆ONSD.
Awake investigation does not impair the correlation between ONSD and ICP. Even if there is a good overall ONSD-ICP correlation, every individual has its own distinctive and precise correlation line. The relationship between ONSD and ICP is furthermore not uniform between individuals. Strong ICP decreases can lead to smaller ONSD changes and vice versa. This should be kept in mind when using this technique in the clinical daily routine.
In the current literature, studies comparing optic nerve sheath diameter (ONSD) with invasive measured intracranial pressure (ICP) revealed a good general correlation of these values in both adult [1,2,3] and pediatric patients [4,5,6]. The largest studies in the pediatric age were performed under general anesthesia either intraoperatively or in patients at the intensive care unit (ICU) . Furthermore, ICP measurement was limited to intraparenchymal probes or determination via intraventricular catheter. Smaller studies either included only a very limited cohort of children with pseudotumor cerebri (PTC), in whom ICP was evaluated via lumbar puncture (LP)  or ICP measurement was restricted to intraparenchymal probes and LP in a small pediatric cohort . Since the goal of a non-invasive technique is to avoid invasive diagnostics and anesthesia, it is essential to investigate patients awake and analyze if wakefulness influences the correlation between ONSD and ICP. Furthermore, there are many possibilities to determine ICP in the clinical daily routine; therefore, it is necessary to investigate if the ONSD-ICP correlation differs between various methods of ICP measurement.
Finally, there is reason to believe that the relationship between ONSD and ICP is not strictly linear. According to a hysteresis theory, reversibility of ONSD could be impaired after extended episodes of ICP increase  and thus lead to persisting abnormal ONSD values under normal ICP conditions. There are moreover hints of our recently published study  and other current studies  that the kind of the underlying pathology might influence the ONSD-ICP correlation as well. Age, patency of anterior fontanelle (AF) , and mobility of skull bones  seem to affect the relationship between ONSD and ICP as well.
Another important precondition for a clinical routine application of ONSD to assess ICP qualitatively is knowledge about dynamic changes of ONSD and ICP after therapy. Even if quick and dynamic regressions of ONSD after ICP decreasing therapy were described in adult patients [11, 12], these dynamics following therapy very likely differ between individuals.
This study aims to investigate the influence of wakefulness and mode of ICP measurement on the ONSD-ICP correlation, dynamic changes of ONSD after ICP decreasing therapy, and intra-individual ONSD-ICP correlations.
This study was performed as a retrospective, observational study.
Ultrasound of the ONSD is part of our daily routine diagnostic workup in all children presenting with suspicion of ICP increase.
Pediatric patients between newborn and 18 years, treated at the University Hospital of Tuebingen, Department of Neurosurgery, Division of Pediatric Neurosurgery between January 2016 and January 2018, were enrolled into the study if they underwent a diagnostic or surgical procedure for diagnosis or therapy of a neurosurgical pathology including invasive ICP measurement and a concurrent ultrasound measurement of the ONSD.
The study was approved by the institutional ethics committee (project number: 180/2018B02).
Patients were included in the study when they underwent a procedure where ICP could be measured safely.
Patients that received ketamine for sedation to tolerate invasive ICP measurement were excluded from the study as ketamine is known to induce ICP increases in spontaneously breathing patients.
The overall cohort included 72 patients with a mean age of 5.2 years, 51 children were > 1 year, and 21 ≤ 1 year. Ten patients presented with an open anterior fontanelle. Fifty children were male (69.4%), and 22 were female (30.6%).
Diagnoses encompassed hydrocephalus (41.7%), craniosynostosis (22.3%), pseudotumor cerebri (13.8%), traumatic brain injury (9.7%), tumor (5.6%), and other intracranial pathologies, such as cysts or subdural hematoma (6.9%).
Forty percent of the patients were investigated intraoperatively under general anesthesia, 39% were awake, 14% were analgo-sedated with propofol/midazolam for lumbar or reservoir puncture, and 7% were somnolent or comatose on intensive care unit. Ketamine, which is known to increase ICP in spontaneously breathing patients, was not used for sedation.
Ultrasound ONSD measurement
Ultrasound measurement of the optic nerve sheath diameter was performed using the same protocol as described in part I of this study . Briefly, three measurements were acquired in an axial plane and the mean ONSD of each side and the mean binocular ONSD was calculated. The mean binocular ONSD was measured and compared to invasively measured ICP at the same time. One examiner (SRK) trained in transorbital ultrasound diagnostics of the ONS performed all ultrasound investigations. The images were saved in jpeg and Dicom format.
Invasive ICP measurement
ICP measurement was performed via intraparenchymal ICP probe (29%), closed extraventricular drainage (EVD) (7%), or puncture of the shunt reservoir (15.3%)/lumbar CSF space (8.4%) in children awake or analgo-sedated. During surgery, ICP was measured using an intraventricular brain needle (25%) or an epidural probe (15.3%).
Data were tested for normality of distribution using Kolmogorov-Smirnov or Shapiro-Wilk test. Parametric data were reported as means and standard deviation (sd). The analyses were done using SPSS (PASW Statistics 18, IBM) statistical software. Depending on normality of distribution, the correlation of the variables was tested using Pearson’s or Spearman’s correlation coefficient. Bland-Altman’s analysis was used to test correlation within subjects. Statistical significance was set at p < 0.05. The independent Student’s t test was used for comparing mean values.
Influence of mode of sedation and wakefulness on ONSD-ICP correlation
The overall cohort included 72 patients. The patients were allocated into subgroups regarding mode of sedation and wakefulness. US-based ONSD was measured simultaneously with invasive ICP measurement.
In the cohort, that was investigated intraoperatively under general anesthesia (n = 29), median age was 6 months, and 31% of the patients had a patent AF. The correlation of ONSD and ICP was poor (r = 0.35, p > 0.05). The correlation improved considerably when excluding the patients with patent AF (n = 20, r = 0.47, p < 0.05; Fig. 1a).
The ONSD-ICP correlation for analgo-sedated and comatose patients (n = 15, median age 6 years, patent AF 2.3%) was good with r = 0.524 (p < 0.05; Fig. 1b).
When only considering those 28 patients that were investigated awake (median age 9 years, patent AF 0%), the correlation between ONSD and ICP was even better (r = 0.802, p < 0.01; Fig. 1c).
Influence of method of ICP measurement on ONSD-ICP correlation
The overall cohort (n = 72) was divided into subgroups regarding different methods of ICP measurement. ONSD and ICP were measured concurrently.
The largest group of patients received an intraparenchymal ICP probe (n = 21, median age 6 years, patency of AF 4.8%); ONSD-ICP correlation was good in this subgroup (r = 0.589, p < 0.01).
In 18 children, median age 1.25 years, ICP measurement was performed intraoperatively via brain needle connected to a manometer line. Correlation between ONSD and ICP was poor in this group (r = 0.313), but the rate of patients with patent AF was 38.9%. A similar poor ONSD-ICP correlation was found in those patients (n = 6) that underwent lumbar puncture (r = 0.301) but in that cohort median age was 6 years and none of them had a patent AF.
Eleven children, median age 0.5 years, underwent intraoperative ICP measurement using an epidural probe. The ONSD-ICP correlation was good (r = 0.585) despite young age and patent AF in 18.1% of these individuals.
A satisfying correlation (r = 0.462) was found in patients, which received a transducer-based ICP measurement during a shunt infusion investigation (n = 7, median age 10).
The best correlation of ONSD and ICP was found in patients, in which ICP determination was performed via puncture of shunt reservoir (r = 0.762; n = 4, median age 9.5) or via closed external ventricular drainage (EVD) (r = 0.916, p < 0.05; n = 5, median age 12).
Dynamics of individual ONSD and ICP changes after ICP decreasing therapy
Thirty children of the entire cohort underwent simultaneous ONSD and ICP measurement before and after an ICP decreasing therapy. Diagnoses encompassed craniosynostosis (n = 8), hydrocephalus (n = 7), PTC (n = 4), tumor (n = 1), patients on ICU (n = 7), and with various intracranial pathologies (n = 3). Measurements were done straight before and after therapy in 21/30 cases and within a maximum of 3–4 days after surgery in 9/30 cases, depending on the child’s condition. Sixty single ICP measurements and 360 ONSD investigations were therefore included. Eleven patients were ≤ 1 year (patency of AF in 4) and 19 > 1 year.
Mean ONSD and ICP values before therapy were 5.7 ± 0.69 mm and 19.6 ± 9.5 mmHg (mean ± sd) and 5.0 ± 0.58 mm and 9.3 ± 7.5 mmHg after therapy, respectively (p < 0.001) (Fig. 2).
Mean difference of ONSD before and after therapy (∆ONSD) was 0.7 ± 0.33 mm and ∆ICP was 10.3 ± 6.8 mmHg.
Correlation of ∆ONSD and ∆ICP was poor for the entire cohort of 30 patients (r = 0.16, p > 0.05) (Fig. 3a), indicating that strong ONSD decreases after therapy can be associated with small ICP decreases and vice versa.
Comparing the correlation of ∆ONSD and ∆ICP according to underlying pathologies, patients with hydrocephalus (n = 7) revealed the poorest correlation (r = − 0.126), followed by patients with craniosynostosis (n = 8; r = 0.312) and patients from ICU (n = 7, r = 0.379).
Children with arachnoid cysts (n = 2) or intracranial bleeding due to compromised coagulation (n = 1) summarized as “various” had a better correlation (n = 3, r = 0.536), and in 4 patients with pseudotumor cerebri, the correlation was surprisingly outstanding (r = 0.997, p < 0.01; Fig. 3b).
Intra-individual ONSD-ICP correlation
Ten patients underwent repeated concurrent ONSD and ICP measurements with a minimum of three measurements. This cohort included six male and four female patients, aged 1.7 to 18 years (median age 4 years) and diagnoses encompassed tumor (n = 3), traumatic brain injury (TBI) (n = 4), pseudotumor cerebri (PTC) (n = 2), and hydrocephalus (n = 1). Intervals of investigation ranged between a few days (tumor and TBI) to a few weeks (PTC) and months (hydrocephalus) depending on pathology and treatment. None of the included patients had a patent AF.
Overall correlation within subjects was good, with r = 0.78 (Fig. 4a).
Additionally, correlation-coefficients and correlation-curves for each individual patient were calculated. Individual correlations of ONSD and ICP were excellent and almost linear, correlation-coefficient r ranging from 0.795 to 1.0 (Fig. 4b), even if they differed a lot from each other.
Our study examines the largest reported cohort in the current literature, where ultrasound-based ONSD and invasive ICP measurements were compared in awake children. It is moreover the first one of its kind, which investigates if and how wakefulness and mode of ICP measurement affects relationship of ONSD and ICP in children. It is additionally the first one of its character, where dynamic changes of ONSD and ICP after therapy and intra-individual correlations of ONSD and ICP are described.
Awake ONSD investigation does not impair correlation with ICP
In the current literature, the extensive pilot investigations of Padayachy et al., evaluating the relationship between ultrasound-based ONSD and invasively measured ICP in children, showed a good correlation of both values but were completely performed in children under general anesthesia [4, 5]. One other study performed awake investigations of ONSD in 64 children, but in the majority of the patients, indirect indicators of raised ICP on CT-imaging were used . According to this study, awake investigation was unproblematically tolerated in the cohort aged 0 to 18 years. That is partially consistent with our experiences. In our cohort, newborn babies and children > 3 years were generally compliant to transorbital ultrasound investigations; patience of the examiner was presupposed. Problems regarding incompliance occurred in the age group between 1 and 3 years and sometimes in mentally retarded patients. In cases of impossible investigation due to incompliance, the feed-and-sleep-technique, described as a method for MRI or CT imaging of infants [14,15,16], might be helpful.
Independently of the way how awake ONSD determination is performed in children, an important question is, if wakefulness impairs the correlation of ONSD and ICP.
In our cohort, patients investigated under general anesthesia revealed the poorest correlation of ONSD and ICP (r = 0.35), whereas correlation became better in the cohort investigated comatose and sedated (r = 0.524 p < 0.05). In the sedated cohort, in 6 children, ICP was measured via lumbar puncture in a lateral position. It is known that increased ICP is measured at lumbar puncture in flexed lateral position .
The best ONSD-ICP correlation was found in the cohort investigated under awake conditions (r = 0.802, p < 0.01). However, it has to be considered that age-distribution within different subgroups was not consistent. Based on incompliance of small children to tolerated ONSD investigation, median age of individuals investigated under general anesthesia was considerably lower than in the other subgroups and our data demonstrate that ONSD-ICP correlation improved with median age in the other groups (Table 2). These results indicate, on the one hand, that age has a stronger influence on ONSD-ICP correlation than wakefulness and, on the other hand, that wakefulness certainly does not have a negative impact on the correlation of ICP to ONSD, what originally had been assumed.
Mode of ICP measurement affects the correlation between ONSD and ICP independently of age and patency of AF
There are several different ways to measure ICP invasively in daily clinical practice; however, ICP determination based on closed EVD or intraparenchymal probe is considered as gold standard of ICP measurement [18,19,20]. One current study reports on stronger effects of CSF drainage on ICP measured with EVD than measured with intraparenchymal probe . To our knowledge, there is no study in the current literature, comparing different methods of ICP measurement regarding reliability and validity in children.
When correlating ONSD with invasively measured ICP values as a foundation for the daily application of ONSD, it is fundamental to know if the ONSD-ICP correlation is affected by different modes of ICP determination.
Evaluating the entire cohort of this study (n = 72), the poorest ONSD-ICP correlation was detected in patients, where ICP was determined via lumbar puncture (r = 0.301, median age 6 years, 0% patency of AF) or intraoperative intraventricular brain needle (0.313, median age 1.25 years, 38.9% patency of AF), in both ICP measured with manometer. Age and patency of AF did not seem to play a major influencing role, as both factors were considerably different in both subgroups having a similar poor correlation. A possible explanation is that intraoperative ICP measurement via ventricular brain needle might not be very precise because of possible CSF loss after ventricle puncture and before ICP measurement. Furthermore, in this group, an open AF and thus a higher intracranial compliance was more prevalent.
At lumbar punctures, there is an influence of the very compliant lumbar thecal sac in addition to influences from position , sedation, relaxation of the patient, or possible CO2 retentions due to sedation , which can impact on the ONSD-ICP correlation.
In the subgroup that received ICP measurement using epidural (median age 0.5 years) or intraparenchymal probe (median age 6 years), ONSD-ICP correlation was very similar and satisfying (r = 0.585, r = 0.589). The improved correlation is likely to be attributed to a more accurate and direct ICP measurement that is independent from investigator and surrounding circumstances.
An outstanding ONSD-ICP correlation was detected in the subgroup receiving ICP measurement via a closed EVD (r = 0.916), followed by ICP measurement via puncture of the shunt reservoir (r = 0.762). Despite the small number of subjects in these subgroups, it is conceivable that, based on anatomical conditions , the width of ONS might reflect the pressure directly determined within the ventricular system best than elsewhere. Additionally, measurements via EVD or reservoir puncture are more independent from investigator than intraoperative ventricle puncture.
In summary, these results suggest that besides age and patency of AF, method of ICP determination has a major impact on relationship between ONSD and ICP.
ONSD reacts quickly to ICP decrease, but changes are not necessarily linear
In our cohort, ONSD evaluation was performed immediately before and in 21 cases immediately after ICP decreasing therapy. In 9 cases, post-therapy measurement was done within a maximum of 3–4 days due to reduced condition of the patients straight after surgery. ONSD showed very quick reactions to ICP decrease in all cases (Fig. 2). Recent studies performed in adult patients also described quick and dynamic changes of ONSD after decrease of ICP through lumbar puncture [11, 12]. In one of these studies , patients were divided into 2 groups according to ICP values ((1) ICP between 20 and 30 cm H2O and (2) ICP > 30 cm H2O) and ONSD values were compared to ICP before initial LP and within 1 month. Changes of ONSD and ICP correlated strongly (r = 0.702, p < 0.001), suggesting a rather linear relationship between those values. Similar studies are not yet available for the pediatric cohort until now.
When comparing ∆ONSD and ∆ICP in our cohort, we found a poor correlation of r = 0.16. The scatter plot (Fig. 3a) shows that strong alterations of ONSD can be associated with small changes in ICP and vice versa. Such dynamics were more likely observable than linear patterns of ONSD and ICP changes. The results of part I of this study  and other studies  point out that kind of pathology might influence the relationship between ONSD and ICP. Thus, we investigated if pathology affects the correlation between ∆ONSD and ∆ICP (Fig. 3b). Correlation was poorest for patients with hydrocephalus (r = − 0.126), followed by patients with synostosis and those who were treated on ICU (r = 0.312; r = 0.379). However, an outstanding correlation was surprisingly detected for patients with PTC (r = 0.997, p < 0.01). One explanation for this phenomenon is that in the PTC group, both age (all patients > 1 year and with closed AF) and pathology are very consistent. These factors differ strongly in the hydrocephalus (half of the patients were ≤ 1 year with patent AF, very different modes of hydrocephalus), synostosis (age ≤ 1 year but part of the patients had a patent AF), and ICU group (inhomogeneous pathologies). Independently of the fact that it would be helpful to increase the number of included patients to distinguish between different forms of hydrocephalus, these results strongly suggest an influence of pathology on the relationship of ONSD and ICP.
The relationship between ONSD and ICP is not linear and reveals inter-individual differences due to other influencing factors
Our results indicate that width and dynamics of ONSD changes are influenced not only by ICP but also by age, patency of AF, and type of pathology. Additionally, there are other studies, implying that the duration of the ICP increase , intraocular pressure [25, 26], and a disturbed communication between optic (oSAS) and intracranial subarachnoid spaces (iSAS) [26, 27] might affect the correlation between ONSD and ICP. One study described a kind of an uncoupling of oSAS and iSAS, when ICP is decreasing below a critical breakpoint during CSF shunting . Moreover, there are rare pathologies described in the literature, coming along with widening of ONSD without associated ICP increase, such as ONS ectasia [29, 30] and meningocele [31, 32].
All these issues (see Fig. 5) emphasize the complexity of CSF dynamics within oSAS and iSAS and do suggest that there is no inter-individual, valid, linear relation between ONSD and ICP. Thus, it is impossible to use a general ONSD-ICP correlation-model translating ONS width into ICP numbers in the daily routine.
This is proven by our analysis of 10 children with different diagnoses investigated repeatedly with at least 3 ONSD and ICP pairs at different timepoints. The overall correlation within subjects was very good (r = 0.78, p < 0.01) (Fig. 4a). When we calculated individual correlation-coefficients and regression-curves for each patient, we found outstanding correlations between r = 0.795 and 1.0, demonstrating that each patient has its own, individual, characteristic, and almost linear regression-curve (Fig. 4b). These results indicate that if the personal ICP-ONSD correlation curve of a patient is known, an ONSD value might be “translated” into an ICP value by a “personal” equation. Further research will have to show if these individual correlations remain stable over years.
The correlation between ONSD and ICP in children is negatively influenced by young age and patency of AF and by the mode of ICP measurement. The ONSD-ICP correlation is indeed not negatively affected by awake investigation. Additionally, the relationship of ONSD and ICP is complex. On the one hand, ONSD reacts very quickly and dynamically to ICP changes, but the relationship of dynamic ONSD-ICP changes is influenced by pathology and various other factors as shown in Fig. 5. On the other hand, intra-individual ONSD-ICP correlations are outstanding and theoretically allow calculation of ICP by an individual formula. Based on these results, a general ONSD-ICP correlation can provide a qualitative estimation of ICP in the clinical routine, which is very reliable as a first orientation but cannot be applied in terms of a translation into ICP “numbers” for a single individuum.
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We are deeply indebted to Juergen Beck, MD PhD, University of Bern and Freiburg, who inspired our interest in ultrasound determination of ONSD and to Llewellyn Padayachy, MD PhD, University of CapeTown and Pretoria, for many fruitful discussions over the years.
The study was approved by the institutional ethics committee (project number: 180/2018B02).
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Kerscher, S.R., Schöni, D., Neunhoeffer, F. et al. The relation of optic nerve sheath diameter (ONSD) and intracranial pressure (ICP) in pediatric neurosurgery practice - Part II: Influence of wakefulness, method of ICP measurement, intra-individual ONSD-ICP correlation and changes after therapy. Childs Nerv Syst 36, 107–115 (2020). https://doi.org/10.1007/s00381-019-04336-4
- Optic nerve sheath diameter
- Awake investigation
- Individual correlation